Abstract
Animals often breed in colonies that can vary in size by several orders of magnitude. Colony-size variation is perplexing because individuals in some colony sizes have lower fitness than those in other colony sizes, yet extensive size variation persists in most populations. Natural variation in colony size has allowed us to better quantify the costs and benefits of coloniality, but what causes and maintains size variation is in general unknown. Ecological correlates of colony-size variation potentially include local availability of resources, such as food or nesting sites, and may also reflect individuals’ sorting among colonies (based on life-history traits, morphology, or behavioral propensities) to find the social environment to which they are best suited. Preferences for particular colony sizes are genetically based in some species. The fitness differences observed among colony sizes may reflect unmeasured tradeoffs among life-history components and also could vary temporally or spatially. Colony-size variation might be maintained by fluctuating directional or stabilizing selection that alternately favors individuals in different group sizes and leads to stasis in the colony-size distribution over the long term. Recent focus on the cues individuals use to select breeding habitat (e.g., conspecific attraction, reproductive success of others) does not satisfactorily explain variation in colony size. Costs of dispersal, reliance on imperfect information, and collective nonrandom movement can also lead to colony-size variation in the absence of fitness-based site selection. Our understanding of factors generating and maintaining variation in colony size remains in its infancy and offers many opportunities for future research with broad implications for behavioral ecology.
Similar content being viewed by others
References
Acker P, Grégoire A, Rat M, et al. (2015) Disruptive viability selection on a black plumage trait associated with dominance. J Evol Biol 28:2027–2041
Acquarone C, Cucco M, Malacarne G (2003) Reproduction of the crag martin (Ptyonoprogne rupestris) in relation to weather and colony size. Ornis Fenn 80:79–85
Ainley DG, Ford RG, Brown ED, Suryan RM, Irons DB (2003) Prey resources, competition, and geographic structure of kittiwake colonies in Prince William Sound. Ecology 84:709–723
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383
Altwegg R, Doutrelant C, Anderson MD, Spottiswoode CN, Covas R (2014) Climate, social factors and research disturbance influence population dynamics in a declining sociable weaver metapopulation. Oecologia 174:413–425
Ambrosini R, Bolzern AM, Canova L, Arieni S, Møller AP, Saino N (2002) The distribution and colony size of barn swallows in relation to agricultural land use. J Appl Ecol 39:524–534
Aparicio JM, Bonal R, Muñoz A (2007) Experimental test on public information use in the colonial lesser kestrel. Evol Ecol 21:783–800
Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103b:458–473
Avilés L (1997) Causes and consequences of cooperation and permanent-sociality in spiders. In: Choe J, Crespi B (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp. 476–498
Avilés L, Tufiño P (1998) Colony size and individual fitness in the social spider Anelosimus eximius. Am Nat 152:403–418
Bacon PJ, Andersen-Harild P (1987) Colonial breeding in mute swans (Cygnus olor) associated with an allozyme of lactate dehydrogenase. Biol J Linn Soc 30:193–228
Barta Z, Giraldeau LA (2001) Breeding colonies as information centers: a reappraisal of information-based hypotheses using the producer-scrounger game. Behav Ecol 12:121–127
Baxter GS, Fairweather PG (1998) Does available foraging area, location or colony character control the size of multispecies egret colonies? Wildlife Res 25:23–32
Beauchamp G, Fernández-Juricic E (2005) The group-size paradox: effects of learning and patch departure rules. Behav Ecol 16:352–357
Beauchamp G, Alexander P, Jovani R (2011) Consistent waves of collective vigilance in groups using public information about predation risk. Behav Ecol 23:368–374
Bell WJ (1991) Searching behaviour: the behavioural ecology of finding resources. Chapman and Hall, London
Bell G (2010) Fluctuating selection: the perpetual renewal of adaptation in variable environments. Phil Trans R Soc B 365:87–97
Bengston SE, Jandt JM (2014) The development of collective personality: the ontogenetic drivers of behavioral variation across groups. Front Ecol Evol 2:art81
Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE (2016) Brain size predicts problem-solving ability in mammalian carnivores. Proc Natl Acad Sci USA 113:2532–2537
Bergmüller R, Schürch HIM (2010) Evolutionary causes and consequences of consistent individual variation in cooperative behaviour. Phil Trans R Soc B 365:2751–2764
Bergmüller R, Taborsky M (2010) Animal personality due to social niche specialisation. Trends Ecol Evol 25:504–511
Bilde T, Coates KS, Birkhofer K, Bird T, Maklakov AA, Lubin Y, Avilés L (2007) Survival benefits select for group living in a social spider despite reproductive costs. J Evol Biol 20:2412–2426
Birkhead TR (2014) Stormy outlook for long-term ecology studies. Nature 514:405
Birt VL, Birt TP, Goulet D, Cairns DK, Montevecchi WA (1987) Ashmole’s halo: direct evidence for prey depletion by a seabird. Mar Ecol-Prog Ser 40:205–208
Bonabeau E, Dagorn L, Fréon P (1999) Scaling in animal group-size distributions. Proc Natl Acad Sci USA 96:4472–4477
Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487
Braude S, Tang-Martinez Z, Taylor GT (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behav Ecol 10:345–350
Brown JL (1982) Optimal group size in territorial animals. J Theor Biol 95:793–810
Brown CR (1988) Enhanced foraging efficiency through information centers: a benefit of coloniality in cliff swallows. Ecology 69:602–613
Brown CR, Brown MB (1986) Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67:1206–1218
Brown CR, Brown MB (1996) Coloniality in the cliff swallow: the effect of group size on social behavior. University of Chicago Press, Chicago
Brown CR, Brown MB (2000) Heritable basis for choice of group size in a colonial bird. Proc Natl Acad Sci USA 97:14825–14830
Brown CR, Brown MB (2001) Avian coloniality: progress and problems. Curr Ornithol 16:1–82
Brown CR, Brown MB (2003) Testis size increases with colony size in cliff swallows. Behav Ecol 14:569–575
Brown CR, Brown MB (2004) Empirical measurement of parasite transmission between groups in a colonial bird. Ecology 85:1619–1626
Brown CR, Rannala B (1995) Colony choice in birds: models based on temporally invariant site quality. Behav Ecol Sociobiol 36:221–228
Brown CR, Brown MB, Brazeal KR (2008) Familiarity with breeding habitat improves daily survival in colonial cliff swallows. Anim Behav 76:1201–1210
Brown CR, Brown MB, Danchin E (2000) Breeding habitat selection in cliff swallows: the effect of conspecific reproductive success on colony choice. J Anim Ecol 69:133–142
Brown CR, Brown MB, Raouf SA, Smith LC, Wingfield JC (2005) Steroid hormone levels are related to choice of colony size in cliff swallows. Ecology 86:2904–2915
Brown CR, Brown MB, Roche EA (2013) Spatial and temporal unpredictability of colony size in cliff swallows across 30 years. Ecol Monogr 83:511–530
Brown CR, Brown MB, Roche EA, O’Brien VA, Page CE (2016) Fluctuating survival selection explains variation in avian group size. Proc Natl Acad Sci USA 113:5113–5118
Brown CR, Covas R, Anderson MD, Brown MB (2003) Multistate estimates of survival and movement in relation to colony size in the sociable weaver. Behav Ecol 14:463–471
Brown CR, Roche EA, Brown MB (2014) Variation in age composition among colony sizes in cliff swallows. J Field Ornithol 85:289–300
Brown CR, Roche EA, Brown MB (2015) Parent–offspring resemblance in colony-specific adult survival of cliff swallows. Evol Ecol 29:537–550
Brown CR, Stutchbury BJ, Walsh PD (1990) Choice of colony size in birds. Trends Ecol Evol 5:398–403
Brunton DH (1999) “Optimal” colony size for least terns: an inter-colony study of opposing selection pressures by predators. Condor 101:607–615
Bukacińska M, Bukacińska D, Jabłoński P (1993) Colonial and noncolonial great crested grebes (Podiceps cristatus) at Lake Łuknajno: nest site characteristics, clutch size and egg biometry. Colon Waterbirds 16:111–118
Burger J (1982) The role of reproductive success in colony-site selection and abandonment in black skimmers (Rynchops niger). Auk 99:109–115
Calabuig G, Ortego J, Cordero PJ, Aparicio JM (2010) Colony foundation in the lesser kestrel: patterns and consequences of the occupation of empty habitat patches. Anim Behav 80:975–982
Campbell SP, Witham JW, Hunter ML Jr (2010) Stochasticity as an alternative to deterministic explanations for patterns of habitat use by birds. Ecol Monogr 80:287–302
Carter AJ, Pays O, Goldizen AW (2009) Individual variation in the relationship between vigilance and group size in eastern grey kangaroos. Behav Ecol Sociobiol 64:237–245
Charmantier A, Keyser AJ, Promislow DEL (2007) First evidence for heritable variation in cooperative breeding behaviour. Proc R Soc Lond B 274:1757–1761
Ciprani R, Jaffe K (2005) On the dynamics of grouping. In: Tonella G (ed) Proceedings of the 5th IASTED International Conference on Modelling. Simulation and Optimization. Oranjestad, Aruba, pp. 56–60
Clark CW, Mangel M (1984) Foraging and flocking strategies: information in an uncertain environment. Am Nat 123:626–641
Clutton-Brock TH, Sheldon BC (2010a) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol Evol 25:562–573
Clutton-Brock TH, Sheldon BC (2010b) The seven ages of Pan. Science 327:1207–1208
Cook LF, Toft CA (2005) Dynamics of extinction: population decline in the colonially nesting tricolored blackbird Agelaius tricolor. Bird Conserv Intl 15:73–88
Cooper RJ, Whitmore RC (1990) Arthropod sampling methods in ornithology. Stud Avian Biol 13:29–37
Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739
Danchin E, Wagner RH (1997) The evolution of coloniality: the emergence of new perspectives. Trends Ecol Evol 12:342–347
Danchin E, Boulinier T, Massot M (1998) Conspecific reproductive success and breeding habitat selection: implications for the study of coloniality. Ecology 79:2415–2428
Danchin E, Giraldeau LA, Wagner RH (2008) Animal aggregations: hypotheses and controversies. In: Danchin E, Giraldeau LA, Cézill F (eds) Behavioural ecology. Oxford University Press, Oxford, pp. 503–545
Dardenne S, Ducatez S, Cote J, Poncin P, Stevens VM (2013) Neophobia and social tolerance are related to breeding group size in a semi-colonial bird. Behav Ecol Sociobiol 67:1317–1327
Davis JA, Brown CR (1999) Costs of coloniality and the effect of colony size on reproductive success in purple martins. Condor 101:737–745
de Cara MAR, Pla O, Guinea F, Tella JL (2002) Adaptive learning and coloniality in birds. arXiv:nlin/0207055v1 [nlin.AO]
Di Maggio R, Campobello D, Tavecchia G, Sarà M (2016) Habitat- and density-dependent demography of a colonial raptor in Mediterranean agro-ecosystems. Biol Conserv 193:116–123
Dittmann T, Zinsmeister D, Becker PH (2005) Dispersal decisions: common terns, Sterna hirundo, choose between colonies during prospecting. Anim Behav 70:13–20
Doligez B, Cadet C, Danchin E, Boulinier T (2003) When to use public information for breeding habitat selection? The role of environmental predictability and density dependence. Anim Behav 66:973–988
Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347
Ebensperger LA, Rivera DS, Hayes LD (2012) Direct fitness of group living mammals varies with breeding strategy, climate and fitness estimates. J Anim Ecol 81:1013–1023
Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33
Evans JC, Votier SC, Dall SRX (2016) Information use in colonial living. Biol Rev 91:658–672
Farinha JC, Leitao D (1996) The size of heron colonies in Portugal in relation to foraging habitat. Colon Waterbirds 19(Spec Publ 1):108–114
Farr JA (1977) Social behavior of the golden silk spider, Nephila clavipes (Linnaeus) (Araneae, Araneidae). J Arachnol 4:137–144
Fasola M, Barbieri F (1978) Factors affecting the distribution of heronries in northern Italy. Ibis 120:537–540
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622
Forbes LS, Kaiser GW (1994) Habitat choice in breeding seabirds: when to cross the information barrier. Oikos 70:377–384
Forbes LS, Jajam M, Kaiser GW (2000) Habitat constraints and spatial bias in seabird colony distributions. Ecography 23:575–578
Forero MG, Tella JL, Hobson KA, Bertellotti M, Blanco G (2002) Conspecific food competition explains variability in colony size: a test in Magellanic penguins. Ecology 83:3466–3475
Franklin JF (1989) Importance and justification of long-term studies in ecology. In: Likens GE (ed) Long-term studies in ecology: approaches and alternatives. Springer Verlag, New York, pp. 3–19
Frederiksen M, Bregnballe T (2001) Conspecific reproductive success affects age of recruitment in a great cormorant, Phalacrocorax carbo sinensis, colony. Proc R Soc Lond B 268:1519–1526
Fretwell SD, Lucas HL Jr (1970) On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:1–36
Furness RW, Birkhead TR (1984) Seabird colony distributions suggest competition for food supplies during the breeding season. Nature 311:655–656
Gager Y, Gimenez O, O’Mara MT, Dechmann DKN (2016) Group size, survival and surprisingly short lifespan in socially foraging bats. BMC Ecol 16:art2
Gerard JF, Bideau E, Maublanc ML, Loisel P, Marchal C (2002) Herd size in large herbivores: encoded in the individual or emergent? Biol Bull 202:275–282
Gibbs JP, Kinkel LK (1997) Determinants of the size and location of great blue heron colonies. Colon Waterbirds 20:1–7
Gibbs JP, Woodward S, Hunter ML, Hutchinson AE (1987) Determinants of great blue heron colony distribution in coastal Maine. Auk 104:38–47
Gil D, Biard C, Lacroix A, Spottiswoode CN, Saino N, Puerta M, Møller AP (2007) Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am Nat 169:802–819
Giraldeau LA, Caraco T (1993) Genetic relatedness and group size in an aggregation economy. Evol Ecol 7:429–438
Giraldeau LA, Caraco T (2000) Social foraging theory. Princeton University Press, Princeton, New Jersey
Giraldeau LA, Gillis D (1985) Optimal group size can be stable: a reply to Sibly. Anim Behav 33:666–667
Giraldeau LA, Valone TJ, Templeton JJ (2002) Potential disadvantages of using socially acquired information. Phil Trans R Soc Lond B 357:1559–1566
Gladstone DE (1979) Promiscuity in monogamous colonial birds. Am Nat 114:545–557
Goodson JL, Evans AK, Lindberg L, Allen CD (2005) Neuro-evolutionary patterning of sociality. Proc R Soc Lond B 272:227–235
Goodson JL, Schrock SE, Klatt JD, Kabelik D, Kingsbury MA (2009) Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science 325:862–866
Griesser M, Ma Q, Webber S, Bowgen K, Sumpter DJT (2011) Understanding animal group-size distributions. PLoS ONE 6:e23438
Griffin LR, Thomas CJ (2000) The spatial distribution and size of rook (Corvus frugilegus) breeding colonies is affected by both the distribution of foraging habitat and by intercolony competition. Proc R Soc Lond B 267:1463–1467
Grinsted L, Pruitt JN, Settepani V, Bilde T (2013) Individual personalities shape task differentiation in a social spider. Proc R Soc B 280:20131407
Groothuis TG, Schwabl H (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct Ecol 16:281–289
Haila Y, Nicholls AO, Hanski IK, Raivio S (1996) Stochasticity in bird habitat selection: year-to-year changes in territory locations in a boreal forest bird assemblage. Oikos 76:536–552
Harwood G, Avilés L (2013) Differences in group size and the extent of individual participation in group hunting may contribute to differential prey-size use among social spiders. Biol Lett 9:20130621
Hass CC, Valenzuela D (2002) Anti-predator benefits of group living in white-nosed coatis (Nasua narica). Behav Ecol Sociobiol 51:570–578
Herring G, Ackerman JT (2011) California gull chicks raised near colony edges have elevated stress levels. Gen Comp Endocrinol 173:72–77
Higashi M, Yamamura N (1993) What determines animal group size? Insider-outsider conflict and its resolution. Am Nat 142:553–563
Hodgkin LK, Symonds MRE, Elgar MA (2014) Leaders benefit followers in the collective movement of a social sawfly. Proc R Soc B 281:20141700
Höglund J, Alatalo RV (1995) Leks. Princeton University Press, Princeton, New Jersey
Höglund J, Montgomerie R, Widemo F (1993) Costs and consequences of variation in the size of ruff leks. Behav Ecol Sociobiol 32:31–39
Hoi H, Hoi-Leitner M (1997) An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations. Behav Ecol 8:113–119
Hoogland JL (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behaviour 69:1–35
Hoogland JL, Sherman PW (1976) Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol Monogr 46:33–58
Hoogland JL, Cannon KE, DeBarbieri LM, Manno TG (2006) Selective predation on Utah prairie dogs. Am Nat 168:546–552
Hötker H (2000) Intraspecific variation in size and density of avocet colonies: effects of nest-distances on hatching and breeding success. J Avian Biol 31:387–398
Hunt GL Jr, Schneider DC (1987) Scale-dependent processes in the physical and biological environment of marine birds. In: Croxall JP (ed) Seabirds, feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp. 7–41
Igual JM, Forero MG, Gomez T, Oro D (2007) Can an introduced predator trigger an evolutionary trap in a colonial seabird? Biol Conserv 137:189–196
Ives AR, Klopfer ED (1997) Spatial variation in abundance created by stochastic temporal variation. Ecology 78:1907–1913
Jarman PJ (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267
Jehl JR Jr (1994) Absence of nest density effects in a growing colony of California gulls. J Avian Biol 25:224–230
Johnson DDP, Kays R, Blackwell PG, Macdonald DW (2002) Does the resource dispersion hypothesis explain group living? Trends Ecol Evol 17:563–570
Johst K, Brandl R (1997) The effect of dispersal on local population dynamics. Ecol Model 104:87–101
Jones G (1987) Colonization patterns in sand martins Riparia riparia. Bird Study 34:20–25
Jones TC, Riechert SE (2008) Patterns of reproductive success associated with social structure and microclimate in a spider system. Anim Behav 76:2011–2019
Jones TC, Riechert SE, Dalrymple SE, Parker PG (2007) Fostering model explains variation in levels of sociality in a spider system. Anim Behav 73:195–204
Jovani R, Mavor R (2011) Group size versus individual group size frequency distributions: a nontrivial distinction. Anim Behav 82:1027–1036
Jovani R, Tella JL (2007) Fractal bird nest distribution produces scale-free colony sizes. Proc R Soc Lond B 274:2465–2469
Jovani R, Lascelles B, Garamszegi LZ, Mavor R, Thaxter CB, Oro D (2016) Colony size and foraging range in seabirds. Oikos 125:968–974
Jovani R, Mavor R, Oro D (2008a) Hidden patterns of colony size variation in seabirds: a logarithmic point of view. Oikos 117:1774–1781
Jovani R, Schielzeth H, Mavor R, Oro D (2012) Specificity of grouping behaviour: comparing colony sizes for the same seabird species in distant populations. J Avian Biol 43:397–402
Jovani R, Serrano D, Ursúa E, Tella JL (2008b) Truncated power laws reveal a link between low-level behavioral processes and grouping patterns in a colonial bird. PLoS ONE 3:e1992
Kazama K, Watanuki Y (2010) Individual differences in nest defense in the colonial breeding black-tailed gulls. Behav Ecol Sociobiol 64:1239–1246
Keiser CN, Pruitt JN (2014) Personality composition is more important than group size in determining collective foraging behaviour in the wild. Proc R Soc B 281:20141424
Kenyon JK, Smith BD, Butler RW (2007) Can redistribution of breeding colonies on a landscape mitigate changing predation danger? J Avian Biol 38:541–551
Kharitonov SP, Siegel-Causey D (1988) Colony formation in seabirds. Curr Ornithol 5:223–272
Kildaw SD, Irons DB, Nysewander DR, Buck CL (2005) Formation and growth of new seabird colonies: the significance of habitat quality. Mar Ornithol 33:49–58
Kingsolver JG, Diamond SE (2011) Phenotypic selection in natural populations: what limits directional selection? Am Nat 177:346–357
Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM (2012) Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol Ecol 26:1101–1118
Kramer DL (1985) Are colonies supraoptimal groups? Anim Behav 33:1031–1032
Krieger MJB, Ross KG (2001) Identification of a major gene regulating complex social behavior. Science 295:328–332
Kurvers RHJM, van Oers K, Nolet BA, Jonker RM, van Wieren SE, Prins HHT, Ydenberg RC (2010) Personality predicts the use of social information. Ecol Lett 13:829–837
Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London
Le Coeur C, Thibault M, Pisanu B, Thibault S, Chapuis JL, Baudry E (2015) Temporally fluctuating selection on a personality trait in a wild rodent population. Behav Ecol 26:1285–1291
Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819
Liker A, Bókony V (2009) Larger groups are more successful in innovative problem solving in house sparrows. Proc Natl Acad Sci USA 106:7893–7898
Lubin YD (1974) Adaptive advantages and the evolution of colony formation in Cyrtophora (Araneae: Araneidae). Zool J Linn Soc 54:321–339
Lusseau D, Williams R, Wilson B, Grellier K, Barton TR, Hammond PS, Thompson PM (2004) Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins. Ecol Lett 7:1068–1076
Ma Q, Johansson A, Sumpter DJT (2011) A first principles derivation of animal group size distributions. J Theor Biol 283:35–43
Magrath MJL, Santema P, Bouwman KM, Brinkhuizen DM, Griffith SC, Langmore NE (2009) Seasonal decline in reproductive performance varies with colony size in the fairy martin, Petrochelidon ariel. Behav Ecol Sociobiol 63:661–672
Magurran AE, Seghers BH, Shaw PW, Carvalho GR (1995) The behavioral diversity and evolution of guppy, Poecilia reticulate, populations in Trinidad. Adv Stud Behav 24:155–202
Markham AC, Gesquiere LR, Alberts SC, Altmann J (2015) Optimal group size in a highly social mammal. Proc Natl Acad Sci USA 112:14882–14887
Martinez FA, Marschall EA (1999) A dynamic model of group-size choice in the coral reef fish Dascyllus albisella. Behav Ecol 10:572–577
Martins CIM, Schaedelin FC, Mann M, Blum C, Mandl I, Urban D, Grill J, Schöβwender J, Wagner RH (2012) Exploring novelty: a component trait of behavioural syndromes in a colonial fish. Behaviour 149:215–231
Matthiopoulos J, Harwood J, Thomas L (2005) Metapopulation consequences of site fidelity for colonially breeding mammals and birds. J Anim Ecol 74:716–727
Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6:1084–1090
Millet A, Pelletier F, Bélisle M, Garant D (2015) Patterns of fluctuating selection on morphological and reproductive traits in female tree swallow (Tachycineta bicolor). Evol Biol 42:349–358
Minias P (2014) Evolution of within-colony distribution patterns of birds in response to habitat structure. Behav Ecol Sociobiol 68:851–859
Minias P, Włodarczyk R, Janiszewski T (2015) Opposing selective pressures may act on the colony size in a waterbird species. Evol Ecol 29:283–297
Minias P, Wojczulanis-Jakubas K, Rutkowski R, Kaczmarek K, Janiszewski T (2016) Spatial patterns of extra-pair paternity in a waterbird colony: separating the effects of nesting density and nest site location. Behav Ecol Sociobiol 70:369–376
Mirville MO, Kelley JL, Ridley AR (2016) Group size and associative learning in the Australian magpie (Cracticus tibicen dorsalis). Behav Ecol Sociobiol 70:417–427
Møller AP (2002) Parent-offspring resemblance in degree of sociality in a passerine bird. Behav Ecol Sociobiol 51:276–281
Møller AP (2010) Brain size, head size and behaviour of a passerine bird. J Evol Biol 23:625–635
Morrissey MB, Hadfield JD (2012) Directional selection in temporally replicated studies is remarkably consistent. Evolution 66:435–442
Moss R, Wanless S, Harris MP (2002) How small northern gannet colonies grow faster than big ones. Waterbirds 25:442–448
Neff JA (1937) Nesting distribution of the tri-colored red-wing. Condor 39:61–81
Neff BD, Cargnelli LM, Côté IM (2004) Solitary nesting as an alternative breeding tactic in colonial nesting bluegill sunfish (Lepomis macrochirus). Behav Ecol Sociobiol 56:381–387
Nocera JJ, Forbes GJ, Giraldeau LA (2006) Inadvertent social information in breeding site selection of natal dispersing birds. Proc R Soc Lond B 273:349–355
Nuechterlein GL, Buitron D, Sachs JL, Hughes CR (2003) Red-necked grebes become semicolonial when prime nesting substrate is available. Condor 105:80–94
Nunn CL, Jordán F, McCabe CM, Verdolin JL, Fewell JH (2015) Infectious disease and group size: more than just a numbers game. Phil Trans R Soc B 370:20140111
O’Connell LA, Hofmann HA (2012) Evolution of a vertebrate social decision-making network. Science 336:1154–1157
Olsthoorn JCM, Nelson JB (1990) The availability of breeding sites for some British seabirds. Bird Study 37:145–164
Oppel S, Beard A, Fox D, et al. (2015) Foraging distribution of a tropical seabird supports Ashmole’s hypothesis of population regulation. Behav Ecol Sociobiol 69:915–926
Parejo D, Oro D, Danchin E (2006) Testing habitat copying in breeding habitat selection in a species adapted to variable environments. Ibis 148:146–154
Picman J, Leonard M, Horn A (1988) Antipredation role of clumped nesting by marsh nesting red-winged blackbirds. Behav Ecol Sociobiol 22:9–15
Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris. Funct Ecol 18:58–66
Pruitt JN, Pinter-Wollman N (2015) The legacy effects of keystone individuals on collective behaviour scale to how long they remain in a group. Proc R Soc B 282:20151766
Pruitt JN, Riechert SE (2011) How within-group behavioural variation and task efficiency enhance fitness in a social group. Proc R Soc B 278:1209–1215
Pruitt JN, Grinsted L, Settepani V (2013) Linking levels of personality: personalities of the ‘average’ and ‘most extreme’ group members predict colony-level personality. Anim Behav 86:391–399
Pruitt JN, Iturralde G, Avilés L, Riechert SE (2011) Amazonian social spiders share similar within-colony behavioural variation and behavioural syndromes. Anim Behav 82:1449–1455
Pulliam HR (1973) On the advantages of flocking. J Theor Biol 38:419–422
Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioural ecology, 2nd edn. Sinauer, Sunderlund, Mass, pp. 122–147
Pulliam HR, Millikan GC (1982) Social organization in the nonreproductive season. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 6. Academic Press, New York, pp. 169–197
Purcell J, Avilés L (2007) Smaller colonies and more solitary living mark higher elevation populations of a social spider. J Anim Ecol 76:590–597
Rannala BH, Brown CR (1994) Relatedness and conflict over optimal group size. Trends Ecol Evol 9:117–119
Ranta E (1993) There is no optimal foraging group size. Anim Behav 46:1032–1035
Ranta E, Lindström K (1990) Assortative schooling in three-spined sticklebacks? Ann Zool Fenn 27:67–75
Ranta E, Rita H, Lindström K (1993) Competition versus cooperation: success of individuals foraging alone and in groups. Am Nat 142:42–58
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
Reed JM, Boulinier T, Danchin E, Oring LW (1999) Informed dispersal: prospecting by birds for breeding sites. Curr Ornithol 15:189–259
Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82
Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086
Roche EA, Brown CR (2013) Among-individual variation in vigilance at the nest in colonial cliff swallows. Wilson J Ornithol 125:685–695
Roche EA, Brown CR, Brown MB (2011) Heritable choice of colony size in cliff swallows: does experience trump genetics in older birds? Anim Behav 82:1275–1285
Roche EA, Brown CR, Brown MB, Lear KM (2013) Recapture heterogeneity in cliff swallows: increased exposure to mist nets leads to net avoidance. PLoS ONE 8:e58092
Rodríguez C, Johst K, Bustamante J (2006) How do crop types influence breeding success in lesser kestrels through prey quality and availability? A modelling approach. J Appl Ecol 43:587–597
Royale JA (2009) Analysis of capture-recapture models with individual covariates using data augmentation. Biometrics 65:267–274
Rubenstein DR (2011) Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc Natl Acad Sci USA 108:10816–10822
Russell GJ, Rosales A (2010) Sociability leads to instability: site-switching cascades in a colonial species. Theor Ecol 3:3–12
Rypstra AL (1985) Aggregations of Nephila clavipes (L.) (Araneae, Araneidae) in relation to prey availability. J Arachnol 13:71–78
Sachs JL, Hughes CR, Nuechterlein GL, Buitron D (2007) Evolution of coloniality in birds: a test of hypotheses with the red-necked grebe (Podiceps grisegena). Auk 124:628–642
Safran RJ (2004) Adaptive site selection rules and variation in group size of barn swallows: individual decisions predict population patterns. Am Nat 164:121–131
Safran RJ (2007) Settlement patterns of female barn swallows Hirundo rustica across different group sizes: access to colorful males or favored nests? Behav Ecol Sociobiol 61:1359–1368
Safran RJ, Doerr VAJ, Sherman PW, Doerr ED, Flaxman SM, Winkler DW (2007) Group breeding in vertebrates: linking individual- and population-level approaches. Evol Ecol Res 9:1163–1185
Safran RJ, McGraw KJ, Pilz KM, Correa SM (2010) Egg-yolk androgen and carotenoid deposition as a function of maternal social environment in barn swallows Hirundo rustica. J Avian Biol 41:470–478
Saino N, Martinelli R, Romano M (2008) Ecological and phenological covariates of offspring sex ratio in barn swallows. Evol Ecol 22:659–674
Sallet J, Mars RB, Noonan MP, Andersson JL, O’Reilly JX, Jbabdi S, Croxson PL, Jenkinson M, Miller KL, Rushworth MFS (2011) Social network size affects neural circuits in macaques. Science 334:697–700
Schippers P, Stienen EWM, Schotman AGM, Snep RPH, Slim PA (2011) The consequences of being colonial: Allee effects in metapopulations of seabirds. Ecol Model 222:3061–3070
Schwabl H (1997) The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissensschaften 84:406–408
Schwager M (2005) Climate change, variable colony sizes and temporal autocorrelation: consequences of living in changing environments. Dissertation, University of Potsdam
Sergio F, Penteriani V (2005) Public information and territory establishment in a loosely colonial raptor. Ecology 86:340–346
Serrano D, Tella JL (2007) The role of despotism and heritability in determining settlement patterns in the colonial lesser kestrel. Am Nat 169:E53–E67
Serrano D, Forero MG, Donázar JA, Tella JL (2004) Dispersal and social attraction affect colony selection and dynamics of lesser kestrels. Ecology 85:3438–3447
Serrano D, Oro D, Ursua E, Tella JL (2005) Colony size selection determines adult survival and dispersal preferences: Allee effects in a colonial bird. Am Nat 166:E22–E31
Serrano D, Tella JL, Donázar JA, Pomarol M (2003) Social and individual features affecting natal dispersal in the colonial lesser kestrel. Ecology 84:3044–3054
Serrano D, Tella JL, Forero MG, Donázar JA (2001) Factors affecting breeding dispersal in the facultatively colonial lesser kestrel: individual experience vs. conspecific cues. J Anim Ecol 70:568–578
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Shields WM, Crook JR, Hebblethwaite ML, Wiles-Ehmann SS (1988) Ideal free coloniality in the swallows. In: Slobodchikoff CN (ed) The ecology of social behavior. Academic Press, San Diego, pp. 189–228
Sibly RM (1983) Optimal group size is unstable. Anim Behav 31:947–948
Siegel-Causey D, Kharitonov SP (1990) The evolution of coloniality. Curr Ornithol 7:285–330
Siepielski AM, DiBattista JD, Carlson SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276
Siepielski AM, DiBattista JD, Evans JA, Carlson SM (2011) Differences in the temporal dynamics of phenotypic selection among fitness components in the wild. Proc R Soc B 278:1572–1580
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
Silk JB (2007a) Social components of fitness in primate groups. Science 317:1347–1351
Silk JB (2007b) The adaptive value of sociality in mammalian groups. Phil Trans R Soc B 362:539–559
Sjöberg M, Albrectsen B, Hjältén J (2000) Truncated power laws: a tool for understanding aggregation patterns in animals? Ecol Lett 3:90–94
Smith DRR (1985) Habitat use by colonies of Philoponella republicana (Araneae, Uloboridae). J Arachnol 13:363–373
Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR (2005) Testosterone and group size in cliff swallows: testing the “challenge hypothesis” in a colonial bird. Horm Behav 47:76–82
Snapp BD (1976) Colonial breeding in the barn swallow (Hirundo rustica) and its adaptive significance. Condor 78:471–480
Soutullo A, Limiñana R, Urios V, Surroca M, Gill JA (2006) Density-dependent regulation of population size in colonial breeders: Allee and buffer effects in the migratory Montagu’s harrier. Oecologia 149:543–552
Spottiswoode CN (2007) Phenotypic sorting in morphology and reproductive investment among sociable weaver colonies. Oecologia 154:589–600
Spottiswoode CN (2009) Fine-scale life-history variation in sociable weavers in relation to colony size. J Anim Ecol 78:504–512
Stamps JA (1988) Conspecific attraction and aggregation in territorial species. Am Nat 131:329–347
Stokes DL, Boersma PD (2000) Nesting density and reproductive success in a colonial seabird, the Magellanic penguin. Ecology 81:2878–2891
Switzer PV (1993) Site fidelity in predictable and unpredictable habitats. Evol Ecol 7:533–555
Szabó ZD, Szép T (2010) Breeding dispersal patterns within a large sand martin (Riparia riparia) colony. J Ornithol 151:185–191
Thompson VJ, Munday PL, Jones GP (2007) Habitat patch size and mating system as determinants of social group size in coral-dwelling fishes. Coral Reefs 26:165–174
Tilman D (1989) Ecological experimentation: strengths and conceptual problems. In: Likens GE (ed) Long-term studies in ecology: approaches and alternatives. Springer Verlag, New York, pp. 136–157
Tóth Z, Bókony V, Lendvai AZ, Szabó K, Pénzes Z, Liker A (2009) Effects of relatedness on social-foraging tactic use in house sparrows. Anim Behav 77:337–342
Václav R, Hoi H (2002) Importance of colony size and breeding synchrony on behaviour, reproductive success and paternity in house sparrows Passer domesticus. Folia Zool 51:35–48
Valone TJ, Templeton JJ (2002) Public information for the assessment of quality: a widespread social phenomenon. Phil Trans R Soc Lond B 357:1549–1557
Velando A, Freire J (2001) How general is the central-periphery distribution among seabird colonies? Nest spatial pattern in the European shag. Condor 103:544–554
Votier SC, Bearhop S, Crane JE, Arcos JM, Furness RW (2007) Seabird predation by great skuas Stercorarius skua—intra-specific competition for food? J Avian Biol 38:234–246
Wagner RH (1993) The pursuit of extra-pair copulations by female birds: a new hypothesis of colony formation. J Theor Biol 163:333–346
Ward MP, Semel B, Jablonski C, Deutsch C, Giammaria V, Miller SB, Mcguire BM (2011) Consequences of using conspecific attraction in avian conservation: a case study of endangered colonial waterbirds. Waterbirds 34:476–480
Whittingham LA, Schwabl H (2002) Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav 63:63–67
Wiklund CG, Andersson M (1994) Natural selection of colony size in a passerine bird. J Anim Ecol 63:765–774
Wilder AP, Frick WF, Langwig KE, Kunz TH (2011) Risk factors associated with mortality from white-nose syndrome among hibernating bat colonies. Biol Lett 7:950–953
Williams CK, Lutz RS, Applegate RD (2003) Optimal group size and northern bobwhite coveys. Anim Behav 66:377–387
Wittenberger JF (1981) Animal social behavior. Duxbury Press, Boston
Wittenberger JF, Hunt GL Jr (1985) The adaptive significance of coloniality in birds. In: Farner DS, King JR (eds) Avian biology, vol 8. Academic Press, San Diego, pp. 1–78
Zemel A, Lubin Y (1995) Inter-group competition and stable group sizes. Anim Behav 50:485–488
Acknowledgments
My thoughts on coloniality have been shaped by interactions with many colleagues over the last 35 years, and I thank especially Kathleen Brazeal, Mary Brown, Rita Covas, Etienne Danchin, Jeffrey Davis, John Hoogland, Henry Horn, Amy Moore, Valerie O’Brien, Catherine Page, Bruce Rannala, Scott Robinson, Erin Roche, Daniel Rubenstein, Bridget Stutchbury, Peter Walsh, and David Wilcove. My research has been facilitated by the Cedar Point Biological Station of the University of Nebraska-Lincoln and supported primarily by the National Science Foundation (most recently by DEB-1453971, IOS-1556356). Erin Roche assisted in the analysis of Fig. 1. I thank Roger Jovani, Valerie O’Brien, and two anonymous reviewers for helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. M. Kappeler
Rights and permissions
About this article
Cite this article
Brown, C.R. The ecology and evolution of colony-size variation. Behav Ecol Sociobiol 70, 1613–1632 (2016). https://doi.org/10.1007/s00265-016-2196-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-016-2196-x